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Restriction of Francisella novicida genetic diversity during infection of the vector midgut.

Reif KE, Palmer GH, Crowder DW, Ueti MW, Noh SM - PLoS Pathog. (2014)

Bottom Line: Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host.We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time.Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington, and Paul G. Allen School for Global Animal Health, Washington State University, Pullman, Washington, United States of America; Animal Disease Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Pullman, Washington, United States of America.

ABSTRACT
The genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circulating in an area) by preventing infection or transmission of particular genotypes. Mammalian hosts often act as "ecological filters" for pathogen diversity, where novel variants are frequently eliminated because of stochastic events or fitness costs. However, whether vectors can serve a similar role in limiting pathogen diversity is less clear. Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host. When both mice and ticks were exposed to mixtures of F. novicida genotypes, significantly fewer genotypes co-colonized ticks compared to mice. In both ticks and mice, increased genotypic diversity negatively affected the recovery of available genotypes. Competition among genotypes contributed to the reduction of diversity during infection of the tick midgut, as genotypes not recovered from tick midguts during mixed genotype infections were recovered from tick midguts during individual genotype infection. Mediated by stochastic and selective forces, pathogen genotype diversity was markedly reduced in the tick. We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time. Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

No MeSH data available.


Related in: MedlinePlus

Maintenance of genotypic diversity in mice and ticks over 100 generations.Number of pathogen genotypes per (A) mouse and (B) tick in model simulations with 100 mice and varying vector-to-host ratios. Variation in vector-to-host ratios was simulated by varying the number of ticks from 100 (1∶1 ratio) to 5000 (50∶1 ratio).
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ppat-1004499-g004: Maintenance of genotypic diversity in mice and ticks over 100 generations.Number of pathogen genotypes per (A) mouse and (B) tick in model simulations with 100 mice and varying vector-to-host ratios. Variation in vector-to-host ratios was simulated by varying the number of ticks from 100 (1∶1 ratio) to 5000 (50∶1 ratio).

Mentions: With all model conditions, individual mice harbored greater pathogen genotypic diversity than ticks (Figure 4, S5, S6). Thus, rare pathogen genotypes were more likely to be lost from the vector population than from the mammalian host population. At the population level, vector-to-host ratios strongly influenced the retention of pathogen genotypic diversity (Figure 4). When vector densities declined and vector-to-host ratios approached 1, pathogen genotypic diversity rapidly declined as individual genotypes were lost from the system. In contrast, high vector-to-host ratios increased the retention of genotypic diversity because the filtering effects of individual ticks were reduced due to large population sizes (Figure 4). Variation in vector or host abundance did not influence pathogen genotypic diversity as strongly as vector-to-host ratios; however, in general, larger vector and host populations led to greater maintenance of pathogen genotypic diversity (Figure S5). Initial pathogen genotypic diversity also influenced the number of pathogen genotypes maintained in the vector and host populations (Figure S6). Not surprisingly, both vectors and hosts individually harbored more pathogen genotypes when the number of initial genotypes was greater. However, the proportion of genotypes in the population infecting individual vectors and hosts declined with greater initial pathogen genotypic diversity (Figure S6) as observed in our experiments with large- and small-genotype pools (Figure 2). Thus, the model showed a trade-off between the raw number of pathogen genotypes that infected individual vectors and hosts and the proportion of the pathogen genotype population they represented.


Restriction of Francisella novicida genetic diversity during infection of the vector midgut.

Reif KE, Palmer GH, Crowder DW, Ueti MW, Noh SM - PLoS Pathog. (2014)

Maintenance of genotypic diversity in mice and ticks over 100 generations.Number of pathogen genotypes per (A) mouse and (B) tick in model simulations with 100 mice and varying vector-to-host ratios. Variation in vector-to-host ratios was simulated by varying the number of ticks from 100 (1∶1 ratio) to 5000 (50∶1 ratio).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4231110&req=5

ppat-1004499-g004: Maintenance of genotypic diversity in mice and ticks over 100 generations.Number of pathogen genotypes per (A) mouse and (B) tick in model simulations with 100 mice and varying vector-to-host ratios. Variation in vector-to-host ratios was simulated by varying the number of ticks from 100 (1∶1 ratio) to 5000 (50∶1 ratio).
Mentions: With all model conditions, individual mice harbored greater pathogen genotypic diversity than ticks (Figure 4, S5, S6). Thus, rare pathogen genotypes were more likely to be lost from the vector population than from the mammalian host population. At the population level, vector-to-host ratios strongly influenced the retention of pathogen genotypic diversity (Figure 4). When vector densities declined and vector-to-host ratios approached 1, pathogen genotypic diversity rapidly declined as individual genotypes were lost from the system. In contrast, high vector-to-host ratios increased the retention of genotypic diversity because the filtering effects of individual ticks were reduced due to large population sizes (Figure 4). Variation in vector or host abundance did not influence pathogen genotypic diversity as strongly as vector-to-host ratios; however, in general, larger vector and host populations led to greater maintenance of pathogen genotypic diversity (Figure S5). Initial pathogen genotypic diversity also influenced the number of pathogen genotypes maintained in the vector and host populations (Figure S6). Not surprisingly, both vectors and hosts individually harbored more pathogen genotypes when the number of initial genotypes was greater. However, the proportion of genotypes in the population infecting individual vectors and hosts declined with greater initial pathogen genotypic diversity (Figure S6) as observed in our experiments with large- and small-genotype pools (Figure 2). Thus, the model showed a trade-off between the raw number of pathogen genotypes that infected individual vectors and hosts and the proportion of the pathogen genotype population they represented.

Bottom Line: Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host.We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time.Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington, and Paul G. Allen School for Global Animal Health, Washington State University, Pullman, Washington, United States of America; Animal Disease Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Pullman, Washington, United States of America.

ABSTRACT
The genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circulating in an area) by preventing infection or transmission of particular genotypes. Mammalian hosts often act as "ecological filters" for pathogen diversity, where novel variants are frequently eliminated because of stochastic events or fitness costs. However, whether vectors can serve a similar role in limiting pathogen diversity is less clear. Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host. When both mice and ticks were exposed to mixtures of F. novicida genotypes, significantly fewer genotypes co-colonized ticks compared to mice. In both ticks and mice, increased genotypic diversity negatively affected the recovery of available genotypes. Competition among genotypes contributed to the reduction of diversity during infection of the tick midgut, as genotypes not recovered from tick midguts during mixed genotype infections were recovered from tick midguts during individual genotype infection. Mediated by stochastic and selective forces, pathogen genotype diversity was markedly reduced in the tick. We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time. Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

No MeSH data available.


Related in: MedlinePlus